Reactive oxygen species production by potato tuber mitochondria is modulated by mitochondrially bound hexokinase activity

Plant Physiology

Volumn 149, Issue 2, 2009, Pages 1099-1110

  Camacho Pereira, Juliana ^a   Meyer, Laudiene Evangelista ^a   Machado, Lilia Bender ^a   Oliveira, Marcus Fernandes ^a   Galina, Antonio ^a  

^a Instituto de Bioquímica Médica   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

SACCHAROMYCES CEREVISIAE; SOLANUM TUBEROSUM;

EID: 60249088371     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.108.129247     Document Type: Article

References (61)

1. Akerman KE, Wikströn MK (1976) Safranine as a probe of the mitochondrial membrane potential. FEBS Lett 68: 191-197
2. Arora KK, Pedersen PL (1988) Functional significance of mitochondrial bound hexokinase in tumor cell metabolism: evidence for preferential phosphorylation of glucose by intramitochondrially generated ATP. J Biol Chem 263: 17422-17428
3. Avigad G, Englard S (1968) 5-Keto-D-fructose. V. Phosphorylation by yeast hexokinase. J Biol Chem 243: 1511-1513
4. BeltrandelRio H, Wilson JE (1991) Hexokinase of rat brain mitochondria: relative importance of adenylate kinase and oxidative phosphorylation as sources of substrate ATP, and interaction with intramitochondrial compartments of ATP and ADP. Arch Biochem Biophys 286: 183-194
5. BeltrandelRio H, Wilson JE (1992) Interaction of mitochondrially bound rat brain hexokinase with intramitochondrial compartments of ATP generated by oxidative phosphorylation and creatine kinase. Arch Biochem Biophys 299: 116-124
6. Bernard EA (1975) Hexokinases from yeast. Methods Enzymol 42: 6-20
7. Bolwell GP, Bindschedler LV, Blee KA, Butt VS, Davies DR, Gardner SL, Gerrish C, Minibayeva F (2002) The apoplastic oxidative burst in response to biotic stress in plants: a three-component system. J Exp Bot 53: 1367-1376
8. Bonnefont-Rousselot D (2002) Glucose and reactive oxygen species. Curr Opin Clin Nutr Metab Care 5: 561-568
9. Boveris A, Chance B (1973) The mitochondrial generation of hydrogen peroxide: general properties and effect of hyperbaric oxygen. Biochem J 134: 707-716
10. Brouquisse R, James F, Raymond P, Pradet A (1991) Study of glucose starvation in excised maize root tips. Plant Physiol 96: 619-626
11. Brownlee M (2001) Biochemistry and molecular cell biology of diabetic complications. Nature 414: 813-820
12. Calegario FF, Cosso RG, Fagian MM, Almeida FV, Jardim WF, Jezek P, Arruda P, Vercesi AE (2003) Stimulation of potato tuber respiration by cold stress is associated with an increased capacity of both plant uncoupling mitochondrial protein (PUMP) and alternative oxidase. J Bioenerg Biomembr 35: 211-220
13. Cesar MDC, Wilson JE (2004) All three isoforms of the voltage-dependent anion channel (VDAC1, VDAC2, and VDAC3) are present in mitochondria from bovine, rabbit, and rat brain. Arch Biochem Biophys 422: 191-196
14. Chance B, Sies H, Boveris A (1979) Hydroperoxide metabolism in mammalian organs. Physiol Rev 59: 527-605
15. Claeyssen E, Rivoal J (2007) Isozymes of plant hexokinase: occurrence, properties and functions. Phytochemistry 68: 709-731
16. Considine MJ, Goodman M, Echtay KS, Laloi M, Whelan J, Brand MD, Sweetlove LJ (2003) Superoxide stimulates a proton leak in potato mitochondria that is related to the activity of uncoupling protein. J Biol Chem 278: 22298-22302
17. Couée I, Sulmon C, Gouesbet G, El Amrani A (2006) An involvement of soluble sugars in reactive oxygen species balance and responses to oxidative stress in plants. J Exp Bot 57: 449-459
18. da-Silva WS, Gómez-Puyou A, de Gómez-Puyou MT, Moreno-Sanchez R, De Felice FG, de Meis L, Oliveira MF, Galina A (2004) Mitochondrial bound hexokinase activity as a preventive antioxidant defense: steady-state ADP formation as a regulatory mechanism of membrane potential and reactive oxygen species generation in mitochondria. J Biol Chem 279: 39846-39855
19. da-Silva WS, Rezende GL, Galina A (2001) Subcellular distribution and kinetic properties of cytosolic and on-cytosolic hexokinases in maize seedling roots: implications for hexose phosphorylation. J Exp Bot 52: 1191-1201
20. Damari-Weissler H, Ginzburg A, Gidoni D, Mett A, Krassovskaya I, Weber AP, Belausov E, Granot D (2007) Spinach SoHXK1 is a mitochondria-associated hexokinase. Planta 226: 1053-1058
21. Dennis DT, Green TR (1975) Soluble and particulate glycolysis in developing castor bean endosperm. Biochem Biophys Res Commun 64: 970-975
22. Dieuaide M, Brouquisse R, Pradet A, Raymond P (1992) Increased fatty acid beta-oxidation after glucose starvation in maize root tips. Plant Physiol 99: 595-600
23. Dry IB, Nash D, Wiskich JT (1983) The mitochondrial localization of hexokinase in pea leaves. Planta 158: 152-156
24. Galina A, Logullo C, Souza EF, Rezende GL, da-Silva W (1999) Sugar phosphorylation modulates ADP inhibition of maize mitochondrial hexokinase. Physiol Plant 105: 17-23
25. Galina A, Reis M, Albuquerque MC, Puyou AG, Puyou MT, de Meis L (1995) Different properties of the mitochondrial and cytosolic hexokinases in maize roots. Biochem J 1: 105-112
26. Gechev TS, Van Breusegem F, Stone JM, Denev I, Laloi C (2006) Reactive oxygen species as signals that modulate plant stress responses and programmed cell death. Bioessays 28: 1091-1101
27. Geigenberger R, Stitt M (1993) Sucrose synthase catalyses a readily reversible reaction in vivo in developing potato tubers and other plant tissues. Planta 189: 329-339
28. Gottlob K, Majewski N, Kennedy S, Kandel E, Robey RB, Hay N (2001) Inhibition of early apoptotic events by Akt/PKB is dependent on the first committed step of glycolysis and mitochondrial hexokinase. Genes Dev 15: 1406-1418
29. Graham JW, Williams TC, Morgan M, Fernie AR, Ratcliffe RG, Sweetlove LJ (2007) Glycolytic enzymes associate dynamically with mitochondria in response to respiratory demand and support substrate channeling. Plant Cell 19: 3723-3738
30. Halliwell B, Gutteridge JMC (2007) Free Radicals in Biology and Medicine. Oxford University Press, Oxford
31. Kim M, Lim JH, Ahn CS, Park K, Kim GT, Kim WT, Pai HS (2006) Mitochondria-associated hexokinases play a role in the control of programmed cell death in Nicotiana benthamiana. Plant Cell 18: 2341-2355
32. Korshunov SS, Skulachev VP, Starkov AA (1997) High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria. FEBS Lett 416: 15-18
33. Liu SS (1997) Generating, partitioning, targeting and functioning of superoxide in mitochondria. Biosci Rep 17: 259-272
34. Liu Y, Ren D, Pike S, Pallardy S, Gassmann W, Zhang S (2007) Chloroplast-generated reactive oxygen species are involved in hypersensitive responselike cell death mediated by a mitogen-activated protein kinase cascade. Plant J 51: 941-954
35. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265-275
36. Meyer LE, Machado LB, Santiago AP, da-Silva WS, De Felice FG, Holub O, Oliveira MF, Galina A (2006) Mitochondrial creatine kinase activity prevents reactive oxygen species generation: antioxidant role of mitochondrial kinase-dependent ADP re-cycling activity. J Biol Chem 281: 37361-37371
37. Miernyk JA, Dennis DT (1983) Mitochondrial, plastid, and cytosolic isozymes of hexokinase from developing endosperm of Ricinus communis. Arch Biochem Biophys 226: 458-468
38. Møller IM (2001) Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annu Rev Plant Physiol Plant Mol Biol 52: 561-591
39. Moore CL, Jöbsis FF (1970) Some studies on the control of respiration in rat brain mitochondrial preparations. Arch Biochem Biophys 138: 295-305
40. Morrell S, ap Rees T (1986) Sugar metabolism in developing tubers of Solanum tuberosum. Phytochemistry 25: 1579-1585
41. Nakashima RA, Mangan PS, Colombini M, Pedersen PL (1986) Hexokinase receptor complex in hepatoma mitochondria: evidence from N,N′-dicyclohexylcarbodiimide-labeling studies for the involvement of the pore-forming protein VDAC. Biochemistry 25: 1015-1021
42. Neuburger M, Journet EP, Bligny R, Carde JP, Douce R (1982) Purification of plant mitochondria by isopycnic centrifugation in density gradients of Percoll. Arch Biochem Biophys 217: 312-323
43. Nishikawa T, Edelstein D, Du XL, Yamagishi S, Matsumura T, Kaneda Y, Yorek MA, Beebe D, Oates PJ, Hammes HP, et al (2000) Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature 13: 787-790
44. Pastorino JG, Shulga N, Hoek JB (2002) Mitochondrial binding of hexokinase II inhibits Bax-induced cytochrome c release and apoptosis. J Biol Chem 277: 7610-7618
45. Puntarulo S, Galleano M, Sanchez RA, Boveris A (1991) Superoxide anion and hydrogen peroxide metabolism in soybean embryonic axes during germination. Biochim Biophys Acta 1074: 277-283
46. Renz A, Stitt M (1993) Substrate specificity and product inhibition of different forms of fructokinases and hexokinases in developing potato tubers. Planta 190: 166-175
47. Rezende GL, Logullo C, Meyer L, Machado LB, Oliveira-Carvalho AL, Zingali RB, Cifuentes D, Galina A (2006) Partial purification of tightly bound mitochondrial hexokinase from maize (Zea mays L.) root membranes. Braz J Med Biol Res 39: 1159-1169
48. Rhoads DM, Subbaiah CC (2007) Mitochondrial retrograde regulation in plants. Mitochondrion 7: 177-194
49. Rolland F, Baena-Gonzalez E, Sheen J (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu Rev Plant Biol 57: 675-709
50. Russell JW, Golovoy D, Vincent AM, Mahendru P, Olzmann JA, Mentzer A, Feldman EL (2002) High glucose-induced oxidative stress and mitochondrial dysfunction in neurons. FASEB J 16: 1738-1748
51. Russell JW, Sullivan KA, Windebank AJ, Herrmann DN, Feldman EL (1999) Neurons undergo apoptosis in animal and cell culture models of diabetes. Neurobiol Dis 6: 347-363
52. Schreck R, Baeuerle PA (1991) A role for oxygen radicals as second messengers. Trends Cell Biol 1: 39-42
53. Skulachev VP (1996) Role of uncoupled and non-coupled oxidations in maintenance of safely low levels of oxygen and its one-electron reductants. Q Rev Biophys 29: 169-202
54. Skulachev VP (1997) Membrane-linked systems preventing superoxide formation. Biosci Rep 17: 347-366
55. Smith AM, Ratcliffe RG, Sweetlove LJ (2004) Activation and function of mitochondrial uncoupling protein in plants. J Biol Chem 279: 51944-51952
56. Tiessen A, Hendriks JH, Stitt M, Branscheid A, Gibon Y, Farré EM, Geigenberger P (2002) Starch synthesis in potato tubers is regulated by post-translational redox modification of ADP-glucose pyrophosphorylase: a novel regulatory mechanism linking starch synthesis to the sucrose supply. Plant Cell 14: 2191-2213
57. Turrens JF (1997) Superoxide production by the mitochondrial respiratory chain. Biosci Rep 17: 3-8
58. Vander Heiden MG, Plas DR, Rathmell JC, Fox CJ, Harris MH, Thompson CB (2001) Growth factors can influence cell growth and survival through effects on glucose metabolism. Mol Cell Biol 21: 5899-5912
59. Vercesi AE, Borecký J, Maia Ide G, Arruda P, Cuccovia IM, Chaimovich H (2006) Plant uncoupling mitochondrial proteins. Annu Rev Plant Biol 57: 383-404
60. Vercesi AE, Martins IS, Silva MAP, Leite HMF, Cuccovia IM, Chaimovich H (1995) PUMPing plants. Nature 375: 24
61. Wilson JE (2003) Isozymes of mammalian hexokinase: structure, subcellular localization and metabolic function. J Exp Biol 206: 2049-2057